Prenatal Exposure to PM2.5 and Cardiac Vagal Tone during Infancy: Findings from a Multiethnic Birth Cohort

Abstract

Background: The autonomic nervous system plays a key role in maintaining homeostasis and responding to external stimuli. In adults, exposure to fine particulate matter (${\mathrm{PM}}_{2.5}$) has been associated with reduced heart rate variability (HRV), an indicator of cardiac autonomic control.

Objectives: Our goal was to investigate the associations of exposure to fine particulate matter (${\mathrm{PM}}_{2.5}$) with HRV as an indicator of cardiac autonomic control during early development.

Methods: We studied 237 maternal-infant pairs in a Boston-based birth cohort. We estimated daily residential ${\mathrm{PM}}_{2.5}$ using satellite data in combination with land-use regression predictors. In infants at 6 months of age, we measured parasympathetic nervous system (PNS) activity using continuous electrocardiogram monitoring during the Repeated Still-Face Paradigm, an experimental protocol designed to elicit autonomic reactivity in response to maternal interaction and disengagement. We used multivariable linear regression to examine average ${\mathrm{PM}}_{2.5}$ exposure across pregnancy in relation to PNS withdrawal and activation, indexed by changes in respiration-corrected respiratory sinus arrhythmia (${\text{RSA}}_c$)-an established metric of HRV that reflects cardiac vagal tone. We examined interactions with infant sex using cross-product terms.

Results: In adjusted models we found that a 1-unit increase in ${\mathrm{PM}}_{2.5}$ (in micrograms per cubic meter) was associated with a 3.53% decrease in baseline ${\text{RSA}}_c$ (95% CI: $-6.96$, 0.02). In models examining ${\text{RSA}}_c$ change between episodes, higher ${\mathrm{PM}}_{2.5}$ was generally associated with reduced PNS withdrawal during stress and reduced PNS activation during recovery; however, these associations were not statistically significant. We did not observe a significant interaction between ${\mathrm{PM}}_{2.5}$ and sex.

Discussion: Prenatal exposure to ${\mathrm{PM}}_{2.5}$ may disrupt cardiac vagal tone during infancy. Future research is needed to replicate these preliminary findings. https://doi.org/10.1289/EHP4434.

Figure 1.

Map of predicted ${\mathrm{PM}}_{2.5}$ levels for PRISM study participants during pregnancy. Each point represents residential ${\mathrm{PM}}_{2.5}$ (${\mathrm{\mu }\mathrm{g}/\mathrm{m}}^3$) averaged across pregnancy. ${\mathrm{PM}}_{2.5}$, fine particulate matter; PRISM, PRogramming of Intergenerational Stress Mechanisms.

Figure 2.

Stylized representation of a typical ${\text{RSA}}_{\mathrm{c}}$ response during the Repeated Still-Face Paradigm (SFP-R). The SFP-R is a 10 min, 5-episode procedure ($\text{episodes}=\text{Play}$, ${\text{SF}}_1$, ${\mathrm{R}}_1$, ${\text{SF}}_2$, ${\mathrm{R}}_2$) that is designed to induce moderate stress in the infant via maternal disengagement and reunion. During the Play and Reunion episodes, the mother is instructed to interact with her infant, who is seated in a car seat across from her, as she normally would. During the Still-Face episodes, the mother maintains a neutral facial expression and avoids touching or vocalizing with her infant. PNS, parasympathetic nervous system; ${\mathrm{R}}_1$, first Reunion episode; ${\mathrm{R}}_2$, second Reunion episode; ${\text{RSA}}_{\mathrm{c}}$, respiratory sinus arrhythmia adjusted for total respiratory cycle time (${\mathrm{T}}_{\text{TOT}}$); ${\text{SF}}_1$, first Still-Face episode; ${\text{SF}}_2$, second Still-Face episode.

Figure 3.

Scatter plot of difference in ${\text{RSA}}_{\mathrm{c}}$ ($\mathrm{\Delta }{\text{RSA}}_{\mathrm{c}}$) between sequential SFP-R episodes by ${\mathrm{PM}}_{2.5}$ (${\mathrm{\mu }\mathrm{g}/\mathrm{m}}^3$) among infants enrolled in the Boston-based PRISM study ($n=237$). Plotted $\mathrm{\Delta }{\text{RSA}}_{\mathrm{c}}$ values are residuals from linear regression models between predictors (${\mathrm{PM}}_{2.5}$, infant activity, race/ethnicity, maternal stress, material hardship) and $\mathrm{\Delta }{\text{RSA}}_{\mathrm{c}}$ added to the grand mean $\mathrm{\Delta }{\text{RSA}}_{\mathrm{c}}$ for each episode. The lines correspond to the estimated coefficients in Table 2 and the rug on the x-axis represents the distribution of ${\mathrm{PM}}_{2.5}$ concentrations. ${\mathrm{PM}}_{2.5}$, fine particulate matter; PRISM, PRogramming of Intergenerational Stress Mechanisms; R, Reunion; ${\text{RSA}}_{\mathrm{c}}$, respiratory sinus arrhythmia [in ms/mL corrected for total respiratory cycle time (${\mathrm{T}}_{\text{TOT}}$)]; SF, Still-Face; SFP-R, Repeated Still-Face Paradigm.